Article

Energy efficiency drives the global seasonal distribution of birds

  • Nature Ecology & Evolutionvolume 2pages962969 (2018)
  • doi:10.1038/s41559-018-0556-9
  • Download Citation
Received:
Accepted:
Published:

Abstract

The uneven distribution of biodiversity on Earth is one of the most general and puzzling patterns in ecology. Many hypotheses have been proposed to explain it, based on evolutionary processes or on constraints related to geography and energy. However, previous studies investigating these hypotheses have been largely descriptive due to the logistical difficulties of conducting controlled experiments on such large geographical scales. Here, we use bird migration—the seasonal redistribution of approximately 15% of bird species across the world—as a natural experiment for testing the species–energy relationship, the hypothesis that animal diversity is driven by energetic constraints. We develop a mechanistic model of bird distributions across the world, and across seasons, based on simple ecological and energetic principles. Using this model, we show that bird species distributions optimize the balance between energy acquisition and energy expenditure while taking into account competition with other species. These findings support, and provide a mechanistic explanation for, the species–energy relationship. The findings also provide a general explanation of migration as a mechanism that allows birds to optimize their energy budget in the face of seasonality and competition. Finally, our mechanistic model provides a tool for predicting how ecosystems will respond to global anthropogenic change.

  • Subscribe to Nature Ecology & Evolution for full access:

    $99

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. 1.

    Wright, D. H. Species–energy theory: an extension of species–area theory. Oikos 41, 496–506 (1983).

  2. 2.

    Evans, K. L., Warren, P. H. & Gaston, K. J. Species–energy relationships at the macroecological scale: a review of the mechanisms. Biol. Rev. 80, 1–25 (2005).

  3. 3.

    Lotka, A. Contribution to the energetics of evolution. Proc. Natl Acad. Sci. USA 8, 147–151 (1922).

  4. 4.

    Brown, J. H., Marquet, P. A. & Taper, M. L. Evolution of body size: consequences of an energetic definition of fitness. Am. Nat. 142, 573–584 (1993).

  5. 5.

    Horak, D., Tószögyová, A. & Storch, D. Relative food limitation drives geographical clutch size variation in South African passerines: a large-scale test of Ashmole’s seasonality hypothesis. Glob. Ecol. Biogeogr. 24, 437–447 (2015).

  6. 6.

    Fryxell, J. M. et al. Multiple movement modes by large herbivores at multiple spatiotemporal scales. Proc. Natl Acad. Sci. USA 105, 19114–19119 (2008).

  7. 7.

    Thorup, K. et al. Resource tracking within and across continents in long-distance bird migrants. Sci. Adv. 3, e1601360 (2017).

  8. 8.

    Willig, M., Kaufman, D. M. & Stevens, R. Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis. Annu. Rev. Ecol. Evol. Syst. 34, 273–309 (2003).

  9. 9.

    Grenyer, R. et al. Global distribution and conservation of rare and threatened vertebrates. Nature 444, 93–96 (2006).

  10. 10.

    Rahbek, C. et al. Predicting continental-scale patterns of bird species richness with spatially explicit models. Proc. R. Soc. B. 274, 165–174 (2007).

  11. 11.

    Kirby, J. S. et al. Key conservation issues for migratory land- and waterbird species on the world’s major flyways. Bird Conserv. Int. 18, S49–S73 (2008).

  12. 12.

    Moreau, R. E. The place of Africa in the Palaearctic migration system. J. Anim. Ecol. 21, 250–271 (1952).

  13. 13.

    Herrera, C. M. On the breeding distribution pattern of European migrant birds: Macarthuras theme reexamined. Auk 3, 496–509 (1978).

  14. 14.

    Hurlbert, A. H. & Haskell, J. P. The effect of energy and seasonality on avian species richness and community composition. Am. Nat. 161, 83–97 (2003).

  15. 15.

    Dalby, L., McGill, B. J., Fox, A. D. & Svenning, J.-C. Seasonality drives global-scale diversity patterns in waterfowl (Anseriformes) via temporal niche exploitation. Glob. Ecol. Biogeogr. 23, 550–562 (2014).

  16. 16.

    Somveille, M., Rodrigues, A. S. L. & Manica, A. Why do birds migrate? A macroecological perspective. Glob. Ecol. Biogeogr. 24, 664–674 (2015).

  17. 17.

    Somveille, M., Manica, A., Butchart, S. H. M. & Rodrigues, A. S. L. Mapping global diversity patterns for migratory birds. PLoS ONE 8, e70907 (2013).

  18. 18.

    Jetz, W. & Rahbek, C. Geographic range size and determinants of avian species richness. Science 297, 1548–1551 (2002).

  19. 19.

    Jetz, W., Rahbek, C. & Colwell, R. K. The coincidence of rarity and richness and the potential signature of history in centres of endemism. Ecol. Lett. 7, 1180–1191 (2004).

  20. 20.

    Orme, C. D. L. et al. Global patterns of geographic range size in birds. PLoS Biol. 4, e208 (2006).

  21. 21.

    Fjeldsa, J., Bowie, R. & Rahbek, C. The role of mountain ranges in the diversification of birds. Annu. Rev. Ecol. Evol. Syst. 43, 249–265 (2012).

  22. 22.

    Fretwell, F. in Migrant Birds in the Neotropics: Ecology, Behaviour, Distribution and Conservation (eds Keast, A. & Morton, E.) 517–527 (Smithsonian Institution Press, Washington, DC, 1980).

  23. 23.

    Cox, G. W. The evolution of avian migration systems between temperate and tropical regions of the New World. Am. Nat. 126, 451–474 (1985).

  24. 24.

    Cox, G. W. The role of competition in the evolution of migration. Evolution 22, 180–192 (1968).

  25. 25.

    IPCC Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) (Cambridge Univ. Press, 2013).

  26. 26.

    Haberl, H. et al. Quantifying and mapping the human appropriation of net primary production in Earth's terrestrial ecosystems. Proc. Natl Acad. Sci. USA 104, 12942–12947 (2007).

  27. 27.

    Gilbert, N. I. et al. Are white storks addicted to junk food? Impacts of landfill use on the movement and behaviour of resident white storks (Ciconia ciconia) from a partially migratory population. Mov. Ecol. 4, 7 (2016).

  28. 28.

    Bird Species Distribution Maps of the World (BirdLife International and NatureServe, 2012); http://datazone.birdlife.org/species/requestdis

  29. 29.

    Sahr, K., White, D. & Kimerling, A. J. Geodesic discrete global grid systems. Cartogr. Geogr. Inf. Sci. 30, 121–134 (2003).

  30. 30.

    Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).

  31. 31.

    NASA Earth Observatory Global Maps (NASA, accessed 10 March 2014); http://earthobservatory.nasa.gov/GlobalMaps

  32. 32.

    Damuth, J. Body size in mammals. Nature 290, 699–700 (1981).

  33. 33.

    Damuth, J. Interspecific allometry of population-density in mammals and other animals: the independence of body-mass and population energy-use. Biol. J. Linn. Soc. 31, 193–246 (1987).

  34. 34.

    White, E. P., Ernest, S. K. M., Kerkhoff, A. J. & Enquist, B. J. Relationships between body size and abundance in ecology. Trends Ecol. Evol. 22, 323–330 (2007).

  35. 35.

    Dunning, J. B. (ed.) Handbook of Avian Body Masses (CRC Press, Boca Raton, 1993).

  36. 36.

    Porter, W. P. & Kearney, M. Size, shape, and the thermal niche of endotherms. Proc. Natl Acad. Sci. USA 106, 19666–19672 (2009).

  37. 37.

    Kendeigh, S. C. Tolerance of cold and Bergmann’s rule. Auk 86, 13–25 (1969).

  38. 38.

    Khaliq, I., Hof, C., Prinzinger, R., Böhning-Gaese, K. & Pfenninger, M. Global variation in thermal tolerances and vulnerability of endotherms to climate change. Proc. R. Soc. 281, 20141097 (2014).

  39. 39.

    Scholander, P., Hock, R.., Walters, V., Johnson, F. & Irving, L. Heat regulation in some arctic and tropical mammals and birds. Biol. Bull. 99, 237–258 (1950).

  40. 40.

    H-Acevedo, D. & Currie, D. J. Does climate determine broad-scale patterns of species richness? A test of the causal link by natural experiment. Glob. Ecol. Biogeogr. 12, 461–473 (2003).

  41. 41.

    Davies, R. G. et al. Topography, energy and the global distribution of bird species richness. Proc. R. Soc. B 274, 1189–1197 (2007).

  42. 42.

    Boucher-Lalonde, V., Kerr, J. T. & Currie, D. J. Does climate limit species richness by limiting individual species' ranges? Proc. R. Soc. B 281, 20132695 (2014).

  43. 43.

    Storch, D. et al. Energy, range dynamics and global species richness patterns: reconciling mid-domain effects and environmental determinants of avian diversity. Ecol. Lett. 9, 1308–1320 (2006).

  44. 44.

    Pigot, A. L., Owens, I. P. F. & Orme, C. D. L. The environmental limits to geographic range expansion in birds. Ecol. Lett. 13, 705–715 (2010).

  45. 45.

    Dolman, P. M. & Sutherland, W. J. The response of bird populations to habitat loss. Ibis 137, 38–46 (1994).

  46. 46.

    Goss-Custard, J. D. Competition for food and interference among waders. Ardea 14, 721–739 (1980).

  47. 47.

    Pawar, S., Dell, A. I. & Savage, V. M. Dimensionality of consumer search space drives trophic interaction strengths. Nature 486, 485–489 (2012).

  48. 48.

    Greenberg, R., Ortiz, J. S. & Caballero, C. M. Aggressive competition for critical resources among migratory birds in the neotropics. Bird Conserv. Int. 4, 115–127 (2010).

  49. 49.

    Pele, O. & Werman, M. Fast and robust Earth Mover’s Distances. In Proc. 2009 IEEE 12th Int. Conf. on Computer Vision. 460–467 (IEEE, 2010).

Download references

Acknowledgements

We are grateful to BirdLife International, NatureServe and all the volunteers who collected and compiled the data on the distribution of bird species, and to R. Green, M. Brooke, K. Gaston, B. Sutherland, B. Sheldon and B. Van Doren for discussions. M.S. was funded by an Entente Cordiale scholarship and an Edward Grey Institute postdoctoral fellowship.

Author information

Affiliations

  1. Edward Grey Institute, Department of Zoology, University of Oxford, Oxford, UK

    • Marius Somveille
  2. Department of Zoology, University of Cambridge, Cambridge, UK

    • Marius Somveille
    •  & Andrea Manica
  3. Centre d’Ecologie Fonctionnelle et Evolutive CEFE UMR 5175, CNRS – Université de Montpellier – Université Paul-Valéry Montpellier – EPHE, Montpellier, France

    • Marius Somveille
    •  & Ana S. L. Rodrigues

Authors

  1. Search for Marius Somveille in:

  2. Search for Ana S. L. Rodrigues in:

  3. Search for Andrea Manica in:

Contributions

M.S. conceived the model and developed it with A.M and A.S.L.R. M.S. also performed the analyses with support from A.M., and drafted the paper with conceptual and editorial input from all authors.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Marius Somveille.

Supplementary information

  1. Supplementary Information

    Supplementary Methods, Supplementary Figures 1–11, Supplementary Results, Supplementary References

  2. Reporting Summary